Edited by Gregory D. Edgecombe, The Natural History Museum, London, United Kingdom, and accepted by the Editorial Board January 29, 2016 (received for review November 14, 2015)

Significance

Understanding the evolution of the CNS is fundamental for resolving the phylogenetic relationships within Panarthropoda (Euarthropoda, Tardigrada, Onychophora). The ground pattern of the panarthropod CNS remains elusive, however, as there is uncertainty on which neurological characters can be regarded as ancestral among extant phyla. Here we describe the ventral nerve cord (VNC) in Chengjiangocaris kunmingensis, an early Cambrian euarthropod from South China. The VNC reveals extraordinary detail, including condensed ganglia and regularly spaced nerve roots that correspond topologically to the peripheral nerves of Priapulida and Onychophora. Our findings demonstrate the persistence of ancestral neurological features of Ecdysozoa in early euarthropods and help to reconstruct the VNC ground pattern in Panarthropoda.

Panarthropods are typified by disparate grades of neurological organization reflecting a complex evolutionary history. The fossil record offers a unique opportunity to reconstruct early character evolution of the nervous system via exceptional preservation in extinct representatives. Here we describe the neurological architecture of the ventral nerve cord (VNC) in the upper-stem group euarthropod Chengjiangocaris kunmingensis from the early Cambrian Xiaoshiba Lagerstätte (South China). The VNC of C. kunmingensis comprises a homonymous series of condensed ganglia that extend throughout the body, each associated with a pair of biramous limbs. Submillimetric preservation reveals numerous segmental and intersegmental nerve roots emerging from both sides of the VNC, which correspond topologically to the peripheral nerves of extant Priapulida and Onychophora. The fuxianhuiid VNC indicates that ancestral neurological features of Ecdysozoa persisted into derived members of stem-group Euarthropoda but were later lost in crown-group representatives. These findings illuminate the VNC ground pattern in Panarthropoda and suggest the independent secondary loss of cycloneuralian-like neurological characters in Tardigrada and Euarthropoda.

We thank K.-S. Du and J.-F. He for assistance with fossil collection. B. J. Eriksson (University of Vienna), G. Mayer (University of Leipzig), and G. Bicker (University of Veterinary Medicine Hannover) generously contributed photographic material for Fig. S5. This work was supported by National Natural Science Foundation of China (NSFC) Grants 41472022 and U1402232 (to J.Y. and X.-g.Z.), a research fellowship at Emmanuel College and a Herchel Smith fellowship (both University of Cambridge; to J.O.-H.), and a Ludwig Maximilians Universität München excellent Junior Researcher fund and NSFC Grant 41528202 (to Y.L.).

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Footnotes

1Present address: Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, United Kingdom.